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Research ArticleNew Research, Cognition and Behavior

Contribution of FEF to Attentional Periodicity during Visual Search: A TMS Study

Laura Dugué, Alexy-Assaf Beck, Philippe Marque and Rufin VanRullen
eNeuro 7 June 2019, 6 (3) ENEURO.0357-18.2019; https://doi.org/10.1523/ENEURO.0357-18.2019
Laura Dugué
1Centre National de la Recherche Scientifique (CNRS), Unité Mixte de Recherche 8002, 75006 Paris, France
2Université Paris Descartes, Sorbonne Paris Cité, Integrative Neuroscience and Cognition Center, 75006 Paris, France
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Alexy-Assaf Beck
3Psychological Sciences Research Institute and Institute of Neuroscience, Université de Louvain, B-1348 Louvain-la-Neuve, Belgique
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Philippe Marque
4Médecine Physique et de Réadaption, 31059 Toulouse, France
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Rufin VanRullen
5CNRS, Unité Mixte de Recherche 5549, Faculté de Médecine de Purpan, 31052 Toulouse, France
6Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, 31052 Toulouse, France
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  • Figure 1.
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    Figure 1.

    Experimental protocol. While participants performed a visual search (finding a T letter among L’s), they were stimulated over the right-FEF or the Vertex (control) with a double-pulse of TMS (25 ms interval) applied at random delays between 50 and 450 ms (50 ms increments) after the search array onset.

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    Figure 2.

    TMS modulates attentional search periodically. A, D′ modulations (test–control condition) are represented as a function of TMS latencies from the search array onset. The color lines represent each individual study [yellow, current FEF study; blue, first V1 study (Dugué et al., 2011); red, second V1 study (Dugué et al., 2015a)]. The black line is the average across all three studies. B, Amplitude spectrum obtained by FFT decomposition of the averaged data across the three studies. The red shaded area represents the significant spectral components and the *peak at 6.3 Hz (p < 0.05). C, E, G, represent criterion, hit rates, and false-alarm rates modulations, respectively (same representation as in A). D, F, H, represent their corresponding amplitude spectra. The red shaded area represents the significant spectral components and the *peaks at 6 Hz and 18 Hz for criterion and 5.8 Hz for hit rates (p < 0.05).

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    Figure 3.

    Attentional periodicity in V1 and FEF. For each study, the graphs in the left column represent the amplitude spectra obtained by FFT decomposition of the averaged performance (as per hit rates modulation; see Materials and Methods) across participants. Note the distinct frequency axis in the middle, because of the increased time resolution (and corresponding Nyquist frequency) in that study. The bottom, dashed black line represents the amplitude spectrum of the surrogate distribution. The red shaded area represents the significant spectral components and the *peaks at 6 Hz and 18 Hz for the second V1 study and 6.5 Hz for the FEF study (p < 0.05). The right column represents the phase distribution of the peak frequency across participants. P values are obtained from Rayleigh test for non-uniform distribution of circular data.

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    Table 1.

    TMS studies investigating the role of attention during difficult, visual search tasks

    Stimulation parameters
    StudyBehavioral manipulationTest regionControlType of stimulationStimulation intensitynConclusions
    Ashbridge (1997)Feature: color
    Conjunction:
    color-orientation
    R-PCNo-TMSSingle-pulse at 11 possible delays (from 0 to 200 ms)80% MSI5R-PC involved in conjunction but not feature tasks
    Walsh et al. (1998)Conjunction:
    color-orientation
    R-PCNo-TMSSingle-pulse at 11 possible delays (from 0 to 200 ms)80% MSI3R-PC involved in novel but not learned conjunction tasks
    Juan and Walsh (2003)Feature: color
    Conjunction:
    color-orientation
    V1/V2No-TMS10 Hz for 500 ms and
    Double-pulse (40 or 100 ms interval) at 6 possible delays
    65% MSI8, 6, & 6V1 involved at late delays (feedback) during conjunction but not feature tasks
    Muggleton et al. (2003)Feature: color
    Conjunction:
    color-orientation
    R-FEF
    L-FEF
    Vertex
    V5
    10 Hz for 500 ms65% MSI5FEF is involved in visual selection, in the absence of saccade
    Ellison et al. (2004)Feature: orientation
    Conjunction:
    color-orientation
    R-PPC
    R-STG
    SHAM on R-PPC or R-STGR-PPC: 10 Hz for 500 ms
    R-STG: 4 Hz for 500 ms
    65% MSI5R-PPC involved in conjunction and R-STG in feature
    O’Shea et al. (2004)Conjunction:
    color-orientation
    R-FEFVertex
    V5
    Double-pulse (40 ms interval) at 5 possible delays (from 0 to 120 ms), 40 ms before mask onsetFEF & Vertex: 65% MSI
    V5: 110% phosphene threshold
    12FEF is involved in visual discrimination, in the absence of saccade
    Fuggetta et al. (2006)Conjunction:
    color-orientation
    R-PPCVertexSingle-pulse 100 ms after stimulus onset85% MSI on average7R-PPC involved in conjunction task
    Ellison et al. (2007)Conjunction:
    color-orientation and
    motion-orientation
    R-PPC
    R-V5
    SHAM on R-PPC or
    R-V5
    10 Hz for 500 ms65% MSI7R-PPC involved in color-orientation
    R-V5 in motion-orientation
    Kalla et al. (2008)Conjunction:
    color-orientation
    R-FEF
    R-PPC
    No-TMSDouble-pulse (40 ms interval) at 5 possible delays (from 0 to 200 ms)60% MSI9R-FEF involved earlier than R-PPC in conjunction tasks
    Muggleton et al. (2008)Feature: color
    Conjunction:
    color-orientation
    R-AG
    L-AG
    Vertex
    No-TMS
    10 Hz for 500 ms65% MSI8R-AG but not L-AG involved in conjunction but not feature tasks
    Schindler et al. (2008)Feature: orientation
    Conjunction:
    color-orientation
    R-PPC
    R-STG
    SHAM on R-PPC or R-STGR-PPC: 10 Hz for 500 ms
    R-STG: 4 Hz for 500 ms
    65% MSI5R-STG processes the left part of the search array presented contralateral
    R-PPC involved for left visual field when full-fields array
    Kalla et al. (2009)Feature: color
    Conjunction:
    color-orientation
    DLPFCVertex
    V5
    TBS: 50 Hz bursts at 5 Hz40% MSI12DLPCF involved in conjunction but not feature tasks
    Dugué et al. (2011)Conjunction:
    L vs T and L vs +
    V1/V2Stimulus at non-retinotopic locationDouble-pulse (25 ms interval) at 8 possible delays (from 100 to 450 ms)55% MSI11V1 involved at late delays (feedback) during conjunction but not feature tasks
    Lane et al. (2011)Feature:
    shape
    Conjunction:
    color-orientation
    R-PPCSHAM on R-PPC10 Hz for 500 ms65% MSI12R-PPC involved in conjunction and feature tasks when participants have to point to the target, but only conjunction when button press response
    Muggleton et al. (2011)Conjunction:
    color-orientation
    R-FEF
    L-PPC
    No-TMS10 Hz for 500 ms60% MSI8L-PPC involved when manual motor response required
    Dugué et al. (2015a)Conjunction:
    L vs T and L vs +
    V1/V2Stimulus at non-retinotopic locationDouble-pulse: one at 312.5 ms and one 13 possible delays (from 112.5 to 437.5 ms)55% MSI10V1 involved periodically during conjunction but not feature tasks (∼6 Hz)
    Yan et al. (2016)Feature:
    color
    Conjunction:
    orientation of triangles
    R-DLPFC
    R-PPC
    Vertex on another group of participantsDouble-pulse (100 ms interval) 200 ms before search array onset51% MSI on average16DLPFC is involved in the conjunction search, while the PPC is involved in the feature search
    Present studyConjunction:
    L vs T
    R-FEFVertexDouble-pulse (25 ms interval) at 9 possible delays (from 50 to 450 ms)52% MSI on average21FEF involved periodically during a conjunction task (∼6 Hz)
    • For each study we report the behavioral manipulation, the stimulation parameters: tested region (R, Right; L, Left; V5, MT area; PC, parietal cortex; PPC, posterior parietal cortex; AG, angular gyrus, part of the PPC; STG, superior temporal gyrus; DLPFC, dorsolateral prefrontal cortex, right hemisphere), control condition, type of stimulation (TBS, theta burst stimulation; note: otherwise mentioned, the reference is the onset of the visual stimuli) and the intensity of the stimulation (MSI, maximum output stimulation intensity of the TMS machine), the amount of participants for which data were analyzed (n), and finally, the authors’ conclusions.

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Contribution of FEF to Attentional Periodicity during Visual Search: A TMS Study
Laura Dugué, Alexy-Assaf Beck, Philippe Marque, Rufin VanRullen
eNeuro 7 June 2019, 6 (3) ENEURO.0357-18.2019; DOI: 10.1523/ENEURO.0357-18.2019

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Contribution of FEF to Attentional Periodicity during Visual Search: A TMS Study
Laura Dugué, Alexy-Assaf Beck, Philippe Marque, Rufin VanRullen
eNeuro 7 June 2019, 6 (3) ENEURO.0357-18.2019; DOI: 10.1523/ENEURO.0357-18.2019
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Keywords

  • FEF
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